Biological Altruism

In evolutionary biology, an organism is said to behave
altruistically when its behaviour benefits other organisms, at a cost
to itself. The costs and benefits are measured in terms of
reproductive fitness, or expected number of offspring. So by
behaving altruistically, an organism reduces the number of offspring it
is likely to produce itself, but boosts the number that other organisms
are likely to produce. This biological notion of altruism is not
identical to the everyday concept. In everyday parlance, an action
would only be called ‘altruistic’ if it was done with the
conscious intention of helping another. But in the biological sense
there is no such requirement. Indeed, some of the most interesting
examples of biological altruism are found among creatures that are
(presumably) not capable of conscious thought at all, e.g. insects. For
the biologist, it is the consequences of an action for reproductive
fitness that determine whether the action counts as altruistic, not the
intentions, if any, with which the action is performed.

Altruistic behaviour is common throughout the animal kingdom,
particularly in species with complex social structures. For example,
vampire bats regularly regurgitate blood and donate it to other members
of their group who have failed to feed that night, ensuring they do not
starve. In numerous bird species, a breeding pair receives help in
raising its young from other ‘helper’ birds, who protect
the nest from predators and help to feed the fledglings. Vervet monkeys
give alarm calls to warn fellow monkeys of the presence of predators,
even though in doing so they attract attention to themselves,
increasing their personal chance of being attacked. In social insect
colonies (ants, wasps, bees and termites), sterile workers devote their
whole lives to caring for the queen, constructing and protecting the
nest, foraging for food, and tending the larvae. Such behaviour is
maximally altruistic: sterile workers obviously do not leave any
offspring of their own—so have personal fitness of zero—but their
actions greatly assist the reproductive efforts of the queen.

From a Darwinian viewpoint, the existence of altruism in nature is
at first sight puzzling, as Darwin himself realized. Natural selection
leads us to expect animals to behave in ways that increase their
own chances of survival and reproduction, not those of others.
But by behaving altruistically an animal reduces its own fitness, so
should be at a selective disadvantage vis-à-vis one which
behaves selfishly. To see this, imagine that some members of a group of
Vervet monkeys give alarm calls when they see predators, but others do
not. Other things being equal, the latter will have an advantage. By
selfishly refusing to give an alarm call, a monkey can reduce the
chance that it will itself be attacked, while at the same time
benefiting from the alarm calls of others. So we should expect natural
selection to favour those monkeys that do not give alarm calls over
those that do. But this raises an immediate puzzle. How did the
alarm-calling behaviour evolve in the first place, and why has it not
been eliminated by natural selection? How can the existence of altruism
be reconciled with basic Darwinian principles?

The problem of altruism is intimately connected with questions about
the level at which natural selection acts. If selection acts
exclusively at the individual level, favouring some individual
organisms over others, then it seems that altruism cannot evolve, for
behaving altruistically is disadvantageous for the individual organism
itself, by definition. However, it is possible that altruism may be
advantageous at the group level. A group containing lots of
altruists, each ready to subordinate their own selfish interests for
the greater good of the group, may well have a survival advantage over
a group composed mainly or exclusively of selfish organisms. A process
of between-group selection may thus allow the altruistic behaviour to
evolve. Within each group, altruists will be at a selective
disadvantage relative to their selfish colleagues, but the fitness of
the group as a whole will be enhanced by the presence of altruists.
Groups composed only or mainly of selfish organisms go extinct,
leaving behind groups containing altruists. In the example of the
Vervet monkeys, a group containing a high proportion of alarm-calling
monkeys will have a survival advantage over a group containing a lower
proportion. So conceivably, the alarm-calling behaviour may evolve by
between-group selection, even though within each group, selection
favours monkeys that do not give alarm calls.

The idea that group selection might explain the evolution of
altruism was first broached by Darwin himself. In The Descent of
Man (1871), Darwin discussed the origin of altruistic and
self-sacrificial behaviour among humans. Such behaviour is obviously
disadvantageous at the individual level, as Darwin realized: “he
who was ready to sacrifice his life, as many a savage has been, rather
than betray his comrades, would often leave no offspring to inherit his
noble nature” (p.163). Darwin then argued that self-sacrificial
behaviour, though disadvantageous for the individual
‘savage’, might be beneficial at the group level: “a
tribe including many members who...were always ready to give aid to
each other and sacrifice themselves for the common good, would be
victorious over most other tribes; and this would be natural
selection” (p.166). Darwin's suggestion is that the altruistic
behaviour in question may have evolved by a process of between-group
selection.

The concept of group selection has a chequered and controversial
history in evolutionary biology. The founders of modern
neo-Darwinism—R.A. Fisher, J.B.S.
Haldane and S. Wright—were all aware that
group selection could in principle permit altruistic behaviours to
evolve, but they doubted the importance of this evolutionary
mechanism. Nonetheless, many mid-twentieth century ecologists and
some ethologists, notably Konrad Lorenz, routinely assumed that
natural selection would produce outcomes beneficial for the whole
group or species, often without even realizing that individual-level
selection guarantees no such thing. This uncritical ‘good of the
species’ tradition came to an abrupt halt in the 1960s, due
largely to the work of G.C. Williams (1966) and J. Maynard Smith
(1964). These authors argued that group selection was an inherently
weak evolutionary force, hence unlikely to promote interesting
altruistic behaviours. This conclusion was supported by a number of
mathematical models, which apparently showed that group selection
would only have significant effects for a limited range of parameter
values. As a result, the notion of group selection fell into
widespread disrepute in orthodox evolutionary circles; see Sober and
Wilson 1998, Segestrale 2000, Okasha 2006, Leigh 2010 and Sober 2011 for details of the
history of this debate.

The major weakness of group selection as an explanation of altruism,
according to the consensus that emerged in the 1960s, was a problem
that Dawkins (1976) called ‘subversion from within’; see
also Maynard Smith 1964. Even if altruism is advantageous at the
group level, within any group altruists are liable to be exploited by
selfish ‘free-riders’ who refrain from behaving
altruistically. These free-riders will have an obvious fitness
advantage: they benefit from the altruism of others, but do not incur
any of the costs. So even if a group is composed exclusively of
altruists, all behaving nicely towards each other, it only takes a
single selfish mutant to bring an end to this happy idyll. By virtue of
its relative fitness advantage within the group, the selfish mutant
will out-reproduce the altruists, hence selfishness will eventually
swamp altruism. Since the generation time of individual organisms is
likely to be much shorter than that of groups, the probability that a
selfish mutant will arise and spread is very high, according to this
line of argument. ‘Subversion from within’ is generally
regarded as a major stumbling block for group-selectionist theories
of the evolution of altruism.

If group selection is not the correct explanation for how the
altruistic behaviours found in nature evolved, then what is? In the
1960s and 1970s a rival theory emerged: kin selection or
‘inclusive fitness’ theory, due originally to Hamilton
(1964). This theory, discussed in detail below, apparently showed how
altruistic behaviour could evolve
without the need for group-level selection, and quickly
gained prominence among biologists interested in the evolution of
social behaviour; the empirical success of kin selection theory
contributed to the demise of the group selection concept. However, the
precise relation between kin and group selection is a source of
ongoing controversy (see for example the recent exchange
in Nature between Nowak, Tarnita and Wilson 2010 and Abbot
et. al. 2011). Since the 1990s, proponents of ‘multi-level
selection theory’ have resuscitated a form of group-level
selection—sometimes called ‘new’ group selection—and
shown that it can permit altruism to evolve (cf. Sober and Wilson
1998). But ‘new’ group selection turns out to be
mathematically equivalent to kin selection in most if not all cases,
as a number of authors have emphasized (Grafen 1984, Frank 1998, West
et al. 2007, Lehmann et al. 2007, Marshall 2011); this point was
already appreciated by Hamilton (1975). Since the relation between
‘old’ and ‘new’ group selection is itself a
point of controversy, this explains why disagreement about the
relation between kin and group selection should persist.

The basic idea of kin selection is simple. Imagine a gene which
causes its bearer to behave altruistically towards other organisms,
e.g. by sharing food with them. Organisms without the gene are
selfish—they keep all their food for themselves, and sometimes get handouts
from the altruists. Clearly the altruists will be at a fitness
disadvantage, so we should expect the altruistic gene to be eliminated
from the population. However, suppose that altruists are discriminating
in who they share food with. They do not share with just anybody, but
only with their relatives. This immediately changes things. For
relatives are genetically similar—they share genes with one another.
So when an organism carrying the altruistic gene shares his food, there
is a certain probability that the recipients of the food will also
carry copies of that gene. (How probable depends on how closely related
they are.) This means that the altruistic gene can in principle spread
by natural selection. The gene causes an organism to behave in a way
which reduces its own fitness but boosts the fitness of its
relatives—who have a greater than average chance of carrying the gene
themselves. So the overall effect of the behaviour may be to increase
the number of copies of the altruistic gene found in the next
generation, and thus the incidence of the altruistic behaviour
itself.

Though this argument was hinted at by Haldane in the 1930s, and to a
lesser extent by Darwin in his discussion of sterile insect castes
in The Origin of Species, it was first made explicit by
William Hamilton (1964) in a pair of seminal papers. Hamilton
demonstrated rigorously that an altruistic gene will be favoured by
natural selection when a certain condition, known as
Hamilton's rule, is satisfied. In its simplest version, the
rule states that b > c/r, where c is
the cost incurred by the altruist (the donor), b is the benefit
received by the recipients of the altruism, and r is
the co-efficient of relationship between donor and
recipient. The costs and benefits are measured in terms of
reproductive fitness. The co-efficient of relationship depends on the
genealogical relation between donor and recipient—it is
defined as the probability that donor and recipient share genes at a
given locus that are ‘identical by descent’. (Two genes
are identical by descent if they are copies of a single gene in a
shared ancestor.) In a sexually reproducing diploid species, the value
of r for full siblings is ½, for parents and offspring
½, for grandparents and grandoffspring ¼, for full
cousins 1/8, and so-on. The higher the value of r, the greater
the probability that the recipient of the altruistic behaviour will
also possess the gene for altruism. So what Hamilton's rule tells us
is that a gene for altruism can spread by natural selection, so long
as the cost incurred by the altruist is offset by a sufficient amount
of benefit to sufficiently closed related relatives. The proof of
Hamilton's rule relies on certain non-trivial assumptions; see Frank
1998, Grafen 1985, 2006, Queller 1992a, 1992b, Boyd and McIlreath 2006
and Birch forthcoming for details.

Though Hamilton himself did not use the term, his idea quickly
became known as ‘kin selection’, for obvious reasons. Kin
selection theory predicts that animals are more likely to behave
altruistically towards their relatives than towards unrelated members
of their species. Moreover, it predicts that the degree of
altruism will be greater, the closer the relationship. In the years
since Hamilton's theory was devised, these predictions have been amply
confirmed by empirical work. For example, in various bird species, it
has been found that ‘helper’ birds are much more likely to
help relatives raise their young, than they are to help unrelated
breeding pairs. Similarly, studies of Japanese macaques have shown that
altruistic actions, such as defending others from attack, tend to be
preferentially directed towards close kin. In most social insect
species, a peculiarity of the genetic system known as
‘haplodiploidy’ means that females on average share more
genes with their sisters than with their own offspring. So a female may
well be able to get more genes into the next generation by helping the
queen reproduce, hence increasing the number of sisters she will have,
rather than by having offspring of her own. Kin selection theory
therefore provides a neat explanation of how sterility in the social
insects may have evolved by Darwinian means. (Note, however, that the
precise significance of haplodiploidy for the evolution of worker
sterility is a controversial question; see Maynard Smith and Szathmary
1995 ch.16, Gardner, Alpedrinha and West 2012.)

Kin selection theory is often presented as a triumph of the
‘gene's-eye view of evolution’, which sees organic
evolution as the result of competition among genes for increased
representation in the gene-pool, and individual organisms as mere
‘vehicles’ that genes have constructed to aid their
propagation (Dawkins 1976, 1982). The gene's eye-view is certainly
the easiest way of understanding kin selection, and was employed by
Hamilton himself in his 1964 papers. Altruism seems anomalous from the
individual organism's point of view, but from the gene's point of view
it makes good sense. A gene wants to maximize the number of copies of
itself that are found in the next generation; one way of doing that is
to cause its host organism to behave altruistically towards other
bearers of the gene, so long as the costs and benefits satisfy the
Hamilton inequality. But interestingly, Hamilton showed that kin
selection can also be understood from the organism's point of view.
Though an altruistic behaviour which spreads by kin selection reduces
the organism's personal fitness (by definition), it increases what
Hamilton called the organism's inclusive fitness. An
organism's inclusive fitness is defined as its personal fitness, plus
the sum of its weighted effects on the fitness of every other organism
in the population, the weights determined by the coefficient of
relationship r. Given this definition, natural selection will act to
maximise the inclusive fitness of individuals in the population (Grafen 2006).
Instead of thinking in terms of selfish genes trying to maximize their
future representation in the gene-pool, we can think in terms of
organisms trying to maximize their inclusive fitness. Most people find
the ‘gene's eye’ approach to kin selection heuristically
simpler than the inclusive fitness approach, but mathematically they
are in fact equivalent (Michod 1982, Frank 1998, Boyd and
McIlreath 2006, Grafen 2006).

Contrary to what is sometimes thought, kin selection does not
require that animals must have the ability to discriminate relatives
from non-relatives, less still to calculate coefficients of
relationship. Many animals can in fact recognize their kin, often by
smell, but kin selection can operate in the absence of such an ability.
Hamilton's inequality can be satisfied so long as an animal behaves
altruistically towards others animals that are in fact its
relatives. The animal might achieve this by having the ability
to tell relatives from non-relatives, but this is not the only
possibility. An alternative is to use some proximal indicator of
kinship. For example, if an animal behaves altruistically towards those
in its immediate vicinity, then the recipients of the altruism are
likely to be relatives, given that relatives tend to live near each
other. No ability to recognize kin is presupposed. Cuckoos exploit
precisely this fact, free-riding on the innate tendency of birds to
care for the young in their nests.

Another popular misconception is that kin selection theory is
committed to ‘genetic determinism’, the idea that genes
rigidly determine or control behaviour. Though some sociobiologists
have made incautious remarks to this effect, evolutionary theories of
behaviour, including kin selection, are not committed to it. So long as
the behaviours in question have a genetical component, i.e.
are influenced to some extent by one or more genetic factor, then the
theories can apply. When Hamilton (1964) talks about a gene which
‘causes’ altruism, this is really shorthand for a gene
which increases the probability that its bearer will behave
altruistically, to some degree. This is much weaker than saying that
the behaviour is genetically ‘determined’, and is quite
compatible with the existence of strong environmental influences on the
behaviour's expression. Kin selection theory does not deny the truism
that all traits are affected by both genes and environment. Nor does it
deny that many interesting animal behaviours are transmitted through
non-genetical means, such as imitation and social learning (Avital and
Jablonka 2000).

The importance of kinship for the evolution of altruism is very widely
accepted today, on both theoretical and empirical grounds. However,
kinship is really only a way of ensuring that altruists and recipients
both carry copies of the altruistic gene, which is the fundamental
requirement. If altruism is to evolve, it must be the case that the
recipients of altruistic actions have a greater than average
probability of being altruists themselves. Kin-directed altruism is
the most obvious way of satisfying this condition, but there are other
possibilities too (Hamilton 1975, Sober and Wilson 1998, Bowles and
Gintis 2011, Gardner and West 2011). For example, if the gene that
causes altruism also causes animals to favour a particular feeding
ground (for whatever reason), then the required correlation between
donor and recipient may be generated. It is this correlation, however
brought about, that is necessary for altruism to evolve. This point
was noted by Hamilton himself in the 1970s: he stressed that the
coefficient of relationship of his 1964 papers should really be
replaced with a more general correlation coefficient, which reflects
the probability that altruist and recipient share genes, whether
because of kinship or not (Hamilton 1970, 1972, 1975). This point is
theoretically important, and has not always been recognized; but in
practice, kinship remains the most important source of statistical
associations between altruists and recipients (Maynard Smith 1998,
Okasha 2002, West
et al. 2007).

The fact that correlation between donor and recipient is the key to
the evolution of altruism can be illustrated via a simple ‘one shot’
Prisoner's dilemma game. Consider a large population of organisms who
engage in a social interaction in pairs; the interaction affects their
biological fitness. Organisms are of two types: selfish (S) and
altruistic (A). The latter engage in pro-social behaviour, thus
benefiting their partner but at a cost to themselves; the former do
not. So in a mixed (S,A) pair, the selfish organism does better—he
benefits from his partner's altruism without incurring any
cost. However, (A,A) pairs do better than (S,S) pairs—for the former
work as a co-operative unit, while the latter do not. The interaction
thus has the form of a one-shot Prisoner's dilemma, familiar from game
theory. Illustrative payoff values to each ‘player’, i.e., each partner
in the interaction, measured in units of biological fitness, are shown
in the matrix below.

Player 2

Altruist

Selfish

Player 1

Altruist

11,11

0,20

Selfish

20,0

5,5

Payoffs for (Player 1, Player 2) in units of reproductive
fitness

The question we are interested in is: which type will be favoured by
selection? To make the analysis tractable, we make two simplifying
assumptions: that reproduction is asexual, and that type is perfectly
inherited, i.e., selfish (altruistic) organisms give rise to selfish
(altruistic) offspring. Modulo these assumptions, the evolutionary
dynamics can be determined very easily, simply by seeing whether
the S or the A type has higher fitness, in the
overall population. The fitness of the S
type, W(S), is the weighted average of the payoff to
an S when partnered with an S and the payoff to
an S when partnered with an A, where the weights are
determined by the probability of having the partner in
question. Therefore,

W(S) = 5 * Prob(S partner/S) +
20 * Prob(A partner/S)

(The conditional probabilities in the above expression should be read
as the probability of having a selfish (altruistic) partner, given
that one is selfish oneself.)

Similarly, the fitness of the A type is:

W(A) = 0 * Prob(S partner/A) +
11 * Prob(A partner/A)

From these expressions for the fitnesses of the two types of organism,
we can immediately deduce that the altruistic type will only be
favoured by selection if there is a statistical correlation between
partners, i.e., if altruists have greater than random chance of being
paired with other altruists, and similarly for selfish types. For
suppose there is no such correlation—as would be the case if the
pairs were formed by random sampling from the population. Then, the
probability of having a selfish partner would be the same for
both S and A types, i.e., P(S
partner/S) = P(S partner/A). Similarly,
P(A partner/S) = P(A
partner/A). From these probabilistic equalities, it follows
immediately that W(S) is greater
than W(A), as can be seen from the expressions for
W(S) and W(A) above; so the
selfish type will be favoured by natural selection, and will increase
in frequency every generation until all the altruists are eliminated
from the population. Therefore, in the absence of correlation between
partners, selfishness must win out (cf. Skyrms 1996). This confirms the point noted in
section 2—that altruism can only evolve if there is a statistical
tendency for the beneficiaries of altruistic actions to be altruists
themselves.

If the correlation between partners is sufficiently strong, in this
simple model, then it is possible for the
condition W(A) > W(S) to be
satisfied, and thus for altruism to evolve. The easiest way to see
this is to suppose that the correlation is perfect, i.e., selfish
types are always paired with other selfish types, and ditto for
altruists, so P(S partner/S) = P(A
partner/A) = 1. This assumption implies
that W(A)=11 and W(S)=5, so
altruism evolves. With intermediate degrees of correlation, it is also
possible for the condition W(S)
> W(A) to be satisfied, given the particular
choice of payoff values in the model above.

This simple model also highlights the point made previously, that
donor-recipient correlation, rather than genetic relatedness, is the
key to the evolution of altruism. What is needed for altruism to
evolve, in the model above, is for the probability of having a partner
of the same type as oneself to be sufficiently larger than the
probability of having a partner of opposite type; this ensures that
the recipients of altruism have a greater than random chance of being
fellow altruists, i.e., donor-recipient correlation. Whether this
correlation arises because partners tend to be relatives, or because
altruists are able to seek out other altruists and choose them as
partners, or for some other reason, makes no difference to the
evolutionary dynamics, at least in this simple example.

Altruism is a well understood topic in evolutionary biology; the
theoretical ideas explained above have been extensively analysed,
empirically confirmed, and are widely accepted. Nonetheless, there are
a number of conceptual ambiguities surrounding altruism and related
concepts in the literature; some of these are purely semantic, others
are more substantive. Three such ambiguities are briefly discussed
below; for further discussion, see West et al. 2007, Sachs
et al. 2004 or Lehmann and Keller 2006.

According to the standard definition, a social behaviour counts as
altruistic if it reduces the fitness of the organism performing the
behaviour, but boosts the fitness of others. This was the definition
used by Hamilton (1964), and by many subsequent authors. However,
there is less consensus on how to describe behaviours that boost the
fitness of others but also boost the fitness of the organism
performing the behaviour. As West et al. (2007) note, such
behaviours are sometimes termed ‘co-operative’, but this
usage is not universal; others use ‘co-operation’ to refer
to behaviour that boosts the fitness of others irrespective of its
effect on self; while still others use ‘cooperation’ as a
synonym for altruism. (Indeed, in the simple Prisoner's dilemma game
above, the two strategies are usually called ‘co-operate’
and ‘defect’.) To avoid this confusion, West et
al. (2007) suggest the term ‘mutual benefit’ for
behaviours that benefit both self and other, while Sachs et
al. (2004) suggest ‘byproduct benefit’.

Whatever term is used, the important point is that behaviours that
benefit both self and others can evolve much more easily than
altruistic behaviours, and thus require no special mechanisms such as
kinship. The reason is clear: organisms performing such behaviours
thereby increase their personal fitness, so are at a selective
advantage vis-a-vis those not performing the behaviour. The fact that
the behaviour has a beneficial effect on the fitness of others is a
mere side-effect, or byproduct, and is not part of the explanation for
why the behaviour evolves. For example, Sachs et al. (2004)
note that an action such as joining a herd or a flock may be of this
sort; the individual gains directly, via his reduced risk of
predation, while simultaneously reducing the predation risk of other
individuals. By contrast with an altruistic action, there is no
personal incentive to ‘cheat’, i.e., to refrain from
performing the action, for doing so would directly reduce personal
fitness.

Also indicative of the difference between altruistic behaviour and
behaviour that benefit both self and others is the fact that in the
latter case, though not the former, the beneficiary may be a member of
a different species, without altering the evolutionary dynamics of the
behaviour. Indeed, there are numerous examples where the
self-interested activities of one organism produce an incidental
benefit for a non-conspecific; such behaviours are sometimes called
‘mutualistic’, though again, this is not the only way that
the latter term has been used (West et al. 2007). By
contrast, in the case of altruism, it makes an enormous difference
whether the beneficiary and the donor are con-specifics or not; for
if not, then kin selection can play no role, and it is quite unclear how
the altruistic behaviour can evolve. Unsurprisingly, virtually all the
bona fide examples of biological altruism in the living world involve
donors and recipients that are con-specifics. (Cases of so-called
‘reciprocal altruism’ are sometimes thought to be
exceptions to this generalization; but see section 4 below.)

A quite different ambiguity concerns the distinction between weak and
strong altruism, in the terminology of D.S. Wilson (1977, 1980,
1990). This distinction is about whether the altruistic action entails
an absolute or relative fitness reduction for the donor. To count as
strongly altruistic, a behaviour must reduce the absolute
fitness (i.e., number of offspring) of the donor. Strong altruism is
the standard notion of altruism in the literature, and was assumed
above. To count as weakly altruistic, an action need only reduce
the relative fitness of the donor, i.e., its fitness relative
to that of the recipient. Thus for example, an action which causes an
organism to leave an additional 10 offspring, but causes each
organism(s) with which it interacts to leave an additional 20
offspring, is weakly but not strongly altruistic. The action boosts
the absolute fitness of the ‘donor’, but boosts the
absolute fitness of other organisms by even more, thus reducing the
donor's relative fitness.

Should weakly altruistic behaviours be classified as altruistic or
selfish? This question is not merely semantic; for the real issue is
whether the conditions under which weak altruism can evolve are
relevantly similar to the conditions under which strong altruism can
evolve, or not. Many authors argue that the answer is
‘no’, on the grounds that weakly altruistic behaviours are
individually advantageous, so can evolve with no component of kin
selection or donor-recipient correlation, unlike strongly altruistic
behaviours (Grafen 1984, Nunney 1985, West et
al. 2007). To appreciate this argument, consider a
game-theoretic scenario similar to the one-shot Prisoner's dilemma of
section 4, in which organisms engage in a pair-wise interaction that
affects their fitness. Organisms are of two types, weakly altruistic
(W) and non-altruistic (N). W-types perform
an action that boosts their own fitness by 10 units and the fitness of
their partner by 20 units; N-types do not perform the action. The
payoff matrix is thus:

Player 2

Weak Altruist

Non

Player 1

Weak Altruist

30,30

10,20

Non

20,10

0,0

Payoffs for (Player 1, Player 2) in units of reproductive
fitness

The payoff matrix highlights the fact that weak altruism is
individually advantageous, and thus the oddity of thinking of it it as
altruistic rather than selfish. To see this, assume for a moment that
the game is being played by two rational agents, as in classical game
theory. Clearly, the rational strategy for each individual
is W, for W dominates N. Each individual
gets a higher payoff from playing W
than N, irrespective of what its opponent
does—30 rather than 20 if the opponent plays W, 10 rather
than 0 if the opponent plays N. This captures a clear sense
in which weak altruism is individually advantageous.

In the context of evolutionary game theory, where the game is being
played by pairs of organisms with hard-wired strategies, the
counterpart of the fact that W dominates N is the
fact that W can spread in the population even if pairs are
formed at random (cf. Wilson 1980). To see this, consider the
expressions for the overall population-wide fitnesses of W
and N:

W(W) = 30 * Prob(W partner/W) + 10
* Prob(N partner/W)

W(N) = 20 * Prob(W partner/N) + 0
* Prob(N partner/N)

(As before, Prob(W partner/W) denotes the
conditional probability of having a weakly altruistic partner given
that one is weakly altruistic oneself, and so-on.) From these
expressions, it is easy to see that W(W)
> W(N) even if the there is no correlation among
partners, i.e., even if Prob(W partner/W) =
P(W partner/N) and P(N partner/W)
= P(N partner/N). Therefore, weak altruism can evolve in the
absence of donor-recipient correlation; as we saw, this is not true of
strong altruism. So weak and strong altruism evolve by different
evolutionary mechanisms, hence should not be co-classified, according
to this argument.

However, there is a counter argument due to D.S. Wilson (1977, 1980),
who maintains that weak altruism cannot evolve by individual selection
alone; a component of group selection is needed. Wilson's argument
stems from the fact that in a mixed (W,N) pair, the
non-altruist is fitter than the weak altruist. More generally, within
a single group of any size containing weak altruists and
non-altruists, the latter will be fitter. So weak altruism can only
evolve, Wilson argues, in a multi-group setting—in which the
within-group selection in favour of N, is counteracted by
between-group selection in favour of W. (On Wilson's view, the
evolutionary game described above is a multi-group setting, involving
a large number of groups of size two.) Thus weak altruism, like strong
altruism, in fact evolves because it is group-advantageous, Wilson
argues.

The dispute between those who regard weak altruism as individually
advantageous, and those like Wilson who regard it as group
advantageous, stems ultimately from differing conceptions of
individual and group selection. For Wilson, individual selection means
within-group selection, so to determine which strategy is favoured by
individual selection, one must compare the fitnesses of W
and N types within a group, or pair. For other theorists,
individual selection means selection based on differences in
individual phenotype, rather than social context; so to determine
which strategy is favoured by individual selection, one must compare
the fitnesses of W and N types in the same social
context, i.e., with the same partner. These two comparisons yield
different answers to the question of whether weak altruism is
individually advantageous. Thus the debate over how to classify weak
altruism is intimately connected to the broader levels of selection
question; see Nunney 1985, Okasha 2005, 2006, Fletcher and Doebeli
2006, West et al. 2007, for further discussion.

A further source of ambiguity in the definition of biological altruism
concerns the time-scale over which fitness is measured. Conceivably,
an animal might engage in a social behaviour which benefits another
and reduces its own (absolute) fitness in the short-term; however, in
the long-term, the behaviour might be to the animal's advantage. So if
we focus on short-term fitness effects, the behaviour will seem
altruistic; but if we focus on lifetime fitness, the behaviour will
seem selfish—the animal's lifetime fitness would be reduced if it
did not perform the behaviour.

Why might a social behaviour reduce an animal's short-term fitness but
boost its lifetime fitness? This could arise in cases of ‘directed
reciprocation’, where the beneficiary of the behaviour returns the
favour at some point in the future (cf. Sachs et al. 2004). By
performing the behaviour, and suffering the short-term cost, the
animal thus ensures (or raises the chance) that it will receive return
benefits in the future. Similarly, in symbioses between members of
different species, it may pay an organism to sacrifice resources for
the benefit of a symbiont with which it has a long-term relationship,
as its long-term welfare may be heavily dependent on the symbiont's
welfare.

From a theoretical point of view, the most satisfactory resolution of
this ambiguity is to use lifetime fitness as the relevant parameter
(cf. West et al. 2007) Thus an action only counts as
altruistic if it reduces an organism's lifetime fitness. This
stipulation makes sense, since it preserves the key idea that the
evolution of altruism requires statistical association between donor
and recipient; this would not be true if short-term fitness were used
to define altruism, for behaviours which reduce short-term fitness but
boost lifetime fitness can evolve with no component of kin selection,
or donor-recipient correlation. However, the stipulation has two
disadvantages: (i) it makes it harder to tell whether a given
behaviour is altruistic, since lifetime fitness is notoriously
difficult to estimate; (ii) it has the consequence that most models of
‘reciprocal altruism’ are mis-named.

The theory of reciprocal altruism was originally developed by Trivers
(1971), as an attempt to explain cases of (apparent) altruism among
unrelated organisms, including members of different species. (Clearly,
kin selection cannot help explain altruism among non-relatives.)
Trivers' basic idea was straightforward: it may pay an organism to
help another, if there is an expectation of the favour being returned
in the future. (‘If you scratch my back, I'll scratch
yours’.) The cost of helping is offset by the likelihood of the
return benefit, permitting the behaviour to evolve by natural
selection. Trivers termed with evolutionary mechanism
‘reciprocal altruism’.

For reciprocal altruism to work, there is no need for the two
individuals to be relatives, nor even to be members of the same
species. However, it is necessary that individuals should interact
with each more than once, and have the ability to recognize other
individuals with whom they have interacted in the
past.[1]
If individuals interact only once in their lifetimes and never meet
again, there is obviously no possibility of return benefit, so there
is nothing to be gained by helping another. However, if individuals
encounter each other frequently, and are capable of identifying and
punishing ‘cheaters’ who have refused to help in the past,
then the helping behaviour can evolve. A ‘cheat’ who
refuses to help will ultimately sabotage his own interests, for
although he does not incur the cost of helping others, he forfeits the
return benefits too—others will not help him in the
future. This evolutionary mechanism is most likely to work where
animals live in relatively small groups, increasing the likelihood of
multiple encounters.

As West et al. (2007) and Bowles and Gintis (2011) note, if altruism is defined by reference to
lifetime fitness, then Trivers' theory is not really about the
evolution of altruism at all; for behaviours that evolve via
reciprocation of benefits, as described by Trivers, are ultimately of
direct benefit to the individuals performing them, so do not reduce
lifetime fitness. Despite this consideration, the label ‘reciprocal
altruism’ is well-entrenched in the literature, and the evolutionary
mechanism that it describes is of some importance, whatever it is
called. Where reciprocal altruism is referred to below, it should be
remembered that the behaviours in question are only altruistic in the
short-term.

The concept of reciprocal altruism is closely related to the
Tit-for-Tat strategy in the iterated Prisoner's Dilemma (IPD) from
game theory. In the IPD, players interact on multiple occasions, and
are able to adjust their behaviour depending on what their opponent
has done in previous rounds. There are two possible strategies,
co-operate and defect; the payoff matrix (per interaction) is as in
section 2.1 above. The fact that the game is iterated rather than
one-shot obviously changes the optimal course of action; defecting is
no longer necessarily the best option, so long as the probability of
subsequent encounters is sufficiently high. In their famous computer
tournament in which a large number of strategies were pitted against
each other in the IPD, Axelrod and Hamilton (1981) found that the
Tit-for-Tat strategy yielded the highest payoff. In Tit-For-Tat, a
player follows two basic rules: (i) on the first encounter, cooperate;
(ii) on subsequent encounters, do what your opponent did on the
previous encounter. The success of Tit-for-Tat was widely taken to
confirm the idea that with multiple encounters, natural selection
could favour social behaviours that entail a short-term fitness
cost. Subsequent work in evolutionary game theory, much of it inspired
by Axelrod and Hamilton's ideas, has confirmed that repeated games
permit the evolution of social behaviours that cannot evolve in
one-shot situations (cf. Nowak 2006); this is closely related to the
so-called 'folk theorem' of repeated game theory in economics
(cf. Bowles and Gintis 2011). For a useful discussion of social
behaviour that evolves via reciprocation of benefits, see Sachs
et al. 2004.

Despite the attention paid to reciprocal altruism by theoreticians,
clear-cut empirical examples in non-human animals are relatively few
(Hammerstein 2003, Sachs et al. 2004, Taborsky 2013). This is
probably because the pre-conditions for reciprocal altruism to evolve-
multiple encounters and individual recognition—are not especially
common. However, one possible example is provided by blood-sharing in
vampire bats (Wilkinson 1984, 1990, Carter & Wilkinson 2013). It
is quite common for a vampire bat to fail to feed on a given
night. This is potentially fatal, for bats die if they go without food
for more than a couple of days. On any given night, bats donate blood
(by regurgitation) to other members of their group who have failed to
feed, thus saving them from starvation. Since vampire bats live in
small groups and associate with each other over long periods of time,
the preconditions for reciprocal altruism are likely to be met.
Wilkinson and his colleagues' studies showed that bats tended to share
food with their close associates, and were more likely to share with
others that had recently shared with them. These findings appear to
accord with reciprocal altruism theory.

Trivers (1985) describes an apparent case of reciprocal altruism
between non con-specifics. On tropical coral reefs, various species of
small fish act as ‘cleaners’ for large fish, removing
parasites from their mouths and gills. The interaction is mutually
beneficial—the large fish gets cleaned and the cleaner gets
fed. However, Trivers notes that the large fish sometimes appear to
behave altruistically towards the cleaners. If a large fish is
attacked by a predator while it has a cleaner in its mouth, then it
waits for the cleaner to leave before fleeing the predator, rather
than swallowing the cleaner and fleeing immediately. Trivers explains
the larger fish's behaviour in terms of reciprocal altruism. Since the
large fish often returns to the same cleaner many times over, it pays
to look after the cleaner's welfare, i.e., not to swallow it, even if
this increases the chance of being wounded by a predator. So the
larger fish allows the cleaner to escape, because there is an
expectation of return benefit—getting cleaned again in the
future. As in the case of the vampire bats, it is because the large
fish and the cleaner interact more than once that the behaviour can
evolve.

The evolutionary theories described above, in particular kin
selection, go a long way towards reconciling the existence of altruism
in nature with Darwinian principles. However, some people have felt
these theories in a way devalue altruism, and that the behaviours they
explain are not ‘really’ altruistic. The grounds for this
view are easy to see. Ordinarily we think of altruistic actions as
disinterested, done with the interests of the recipient, rather than
our own interests, in mind. But kin selection theory explains
altruistic behaviour as a clever strategy devised by selfish genes as
a way of increasing their representation in the gene-pool, at the
expense of other genes. Surely this means that the behaviours in
question are only ‘apparently’ altruistic, for they are
ultimately the result of genic self-interest? Reciprocal altruism
theory also seems to ‘take the altruism out of
altruism’. Behaving nicely to someone in order to procure return
benefits from them in the future seems in a way the antithesis of
‘real’ altruism—it is just delayed self-interest.

This is a tempting line of argument. Indeed Trivers (1971) and,
arguably, Dawkins (1976) were themselves tempted by it. But it should
not convince. The key point to remember is that biological altruism
cannot be equated with altruism in the everyday vernacular sense.
Biological altruism is defined in terms of fitness consequences, not
motivating intentions. If by ‘real’ altruism we mean
altruism done with the conscious intention to help, then the vast
majority of living creatures are not capable of ‘real’
altruism nor therefore of ‘real’ selfishness either. Ants
and termites, for example, presumably do not have conscious intentions,
hence their behaviour cannot be done with the intention of promoting
their own self-interest, nor the interests of others. Thus the
assertion that the evolutionary theories reviewed above show that the
altruism in nature is only apparent makes little sense. The contrast
between ‘real’ altruism and merely apparent altruism simply
does not apply to most animal species.

To some extent, the idea that kin-directed altruism is not
‘real’ altruism has been fostered by the use of the
‘selfish gene’ terminology of Dawkins (1976). As we have
seen, the gene's-eye perspective is heuristically useful for
understanding the evolution of altruistic behaviours, especially those
that evolve by kin selection. But talking about ‘selfish’
genes trying to increase their representation in the gene-pool is of
course just a metaphor (as Dawkins fully admits); there is no literal
sense in which genes ‘try’ to do anything. Any
evolutionary explanation of how a phenotypic trait evolves must
ultimately show that the trait leads to an increase in frequency of
the genes that code for it (presuming the trait is transmitted
genetically.) Therefore, a ‘selfish gene’ story can by
definition be told about any trait, including a behavioural trait,
that evolves by Darwinian natural selection. To say that kin selection
interprets altruistic behaviour as a strategy designed by
‘selfish’ genes to aid their propagation is not wrong; but
it is just another way of saying that a Darwinian explanation for the
evolution of altruism has been found. As Sober and Wilson (1998) note,
if one insists on saying that behaviours which evolve by kin selection
/ donor-recipient correlation are ‘really selfish’, one
ends up reserving the word ‘altruistic’ for behaviours
which cannot evolve by natural selection at all.

Do theories of the evolution of biological altruism apply to humans?
This is part of the broader question of whether ideas about the
evolution of animal behaviour can be extrapolated to humans, a
question that fuelled the sociobiology controversy of the 1980s and is
still actively debated today (cf. Boyd and Richerson 2006, Bowles and
Gintis 2011, Sterelny 2012). All biologists accept that Homo sapiens is an
evolved species, and thus that general evolutionary principles apply
to it. However, human behaviour is obviously influenced by culture to
a far greater extent than that of other animals, and is often the
product of conscious beliefs and desires (though this does not
necessarily mean that genetics has no influence.) Nonetheless, at
least some human behaviour does seem to fit the predictions of the
evolutionary theories reviewed above. In general, humans behave more
altruistically (in the biological sense) towards their close kin than
towards non-relatives, e.g. by helping relatives raise their children,
just as kin selection theory would predict. It is also true that we
tend to help those who have helped us out in the past, just as
reciprocal altruism theory would predict. On the other hand, humans
are unique in that we co-operate extensively with our non-kin; and
more generally, numerous human behaviours seem anomalous from the
point of view of biological fitness. Think for example of adoption.
Parents who adopt children instead of having their own reduce their
biological fitness, obviously, so adoption is an altruistic behaviour.
But it is does not benefit kin—for parents are generally
unrelated to the infants they adopt—and nor do the parents
stand to gain much in the form of reciprocal benefits. So although
evolutionary considerations can help us understand some human
behaviours, they must be applied judiciously.

Where human behaviour is concerned, the distinction between biological
altruism, defined in terms of fitness consequences, and
‘real’ altruism, defined in terms of the agent's conscious
intentions to help others, does make sense. (Sometimes the label
‘psychological altruism’ is used instead of
‘real’ altruism.) What is the relationship between these
two concepts? They appear to be independent in both directions, as
Elliott Sober (1994) has argued; see also Vromen (2012) and Clavien and Chapuisat (2013). An action
performed with the conscious intention of helping another human being
may not affect their biological fitness at all, so would not count as
altruistic in the biological sense. Conversely, an action undertaken
for purely self-interested reasons, i.e., without the conscious
intention of helping another, may boost their biological fitness
tremendously.

Sober argues that, even if we accept an evolutionary approach to human
behaviour, there is no particular reason to think that evolution would
have made humans into egoists rather than psychological altruists (see
also Schulz 2011). On the contrary, it is quite possible that natural
selection would have favoured humans who genuinely do care about
helping others, i.e., who are capable of ‘real’ or
psychological altruism. Suppose there is an evolutionary advantage
associated with taking good care of one's children—a quite
plausible idea. Then, parents who
really do care about their childrens' welfare, i.e., who are
‘real’ altruists, will have a higher inclusive fitness,
hence spread more of their genes, than parents who only pretend to
care, or who do not care. Therefore, evolution may well lead
‘real’ or psychological altruism to evolve. Contrary to
what is often thought, an evolutionary approach to human behaviour does
not imply that humans are likely to be motivated by
self-interest alone. One strategy by which ‘selfish genes’
may increase their future representation is by causing humans to be
non-selfish, in the psychological sense.